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The chick embryo is a well-known model for cardiovascular research, in which it is commonly used for the study of cardiac development, though not to date cardiac function. In other animal models, magnetic resonance imaging (MRI) has evolved into a major noninvasive tool to study healthy and diseased hearts, for instance in assessing left ventricular function (ejection fraction, myocardial mass, and wall thickness) and infarct size and in assessing anatomic abnormalities. The lack of MRI application to chick embryos is partly due to the difficulty of monitoring chick ECG and respiration signals, which are conventionally essential in acquiring images free of motion artifact, by prospectively triggering the MR scanner. In the present study, we remove these obstacles by employing a self-gated cine MRI protocol that incorporates a navigator-based retrospective gating technique. The navigator signal is retrospectively used to determine cardiac and respiratory cycles, allowing the MRI k-space data to be reorganized and reconstructed retrospectively, producing cardiac images that are free of motion artifacts. This ability to produce cardiac MRI images without the need for ECG or respiration sensors has allowed noninvasive multislice imaging of the cardiac function of the chick embryo in ovo for the first time (Figures 1 and 2⇓ and online-only Data Supplement Movie I). This technique also offers the possibility to serially image the chick heart through various stages of embryonic development (Figure 3 and online-only Data Supplement Movies II, III, IV, and V). The ability to image the early stages of development is currently limited by the MRI hardware and not by the retrospective gating technique demonstrated here. As MRI technology advances, imaging ever-earlier stages of cardiac development will be possible.

Figure 1. Short-axis MR images of a fully developed chick embryo heart (day 20, stage 46) from base to apex (A through H) taken during diastole. The in-plane image resolution is 300×300 μm, with a slice thickness of 1.5 mm. The heart is one of the first organs to develop, and by as early as day 12 of incubation its conical shape is easily recognizable in MRI scans of fertile eggs. Bar=5 mm.

Figure 3. Short-axis images showing development from day 8 to day 20 of the embryonic chick heart at diastole. The in-plane image resolution is 300×300 μm. Bar=5 mm.

The MRI experiments were performed on a 7T Bruker Biospec system (Bruker Biospec, Karlsruhe, Germany), using a 72-mm birdcage radio frequency volume resonator. The eggs used in the present study were obtained from broiler breeder hens and were at day 8, 13, 16, and 20 of incubation. Each egg was placed into a custom-built polystyrene holder, which was suspended within the resonator/magnet in order to minimize vibrations arising in the gradient coils. A modified fast low-angle shot sequence with an in-slice navigator echo was used for multislice cine MRI. The analysis of the navigator echo and reconstruction of k-space data were performed using PavaVision Intragate (Bruker) software and Fourier filtering techniques.1 The high-quality images of day 20, with in-plane resolution of 300×300 μm and slice thickness of 1.5 mm, were then semiautomatically segmented with the CAAS MRV FARM program (Pie Medical Imaging, Maastricht, the Netherlands), giving global heart parameters such as end-diastolic volume, end-systolic volume, ejection fraction, and wall thickness.

Acknowledgments

This research was supported by a Scottish Higher Education Funding Council grant.

Disclosures

None.

Footnotes

The online-only Data Supplement, which consists of movies, is available with this article at http://circ.ahajournals.org/cgi/content/full/117/21/ e346/DC1.